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Parasite infestation increases on coral reefs without cleaner fish

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Abstract

Mutualisms are pivotal in shaping ecological communities. Iconic images of cleaner fish entering the mouths of predatory fish clients to remove ectoparasites epitomize their mutual benefit. Experimental manipulations of cleaner wrasse reveal declines in fish size and growth, and population abundance and diversity of client fishes in the absence of cleaner wrasse. Fishes grow more slowly and are less abundant and diverse on reefs without cleaner wrasse, both for larger species that are regularly cleaned and have high ectoparasite loads (“attractive species”), and for those smaller species that are rarely cleaned and are rarely infested with parasites (“unattractive species”). We therefore considered whether these previously observed declines in individual and population parameters on reefs without cleaners were related to increased ectoparasite infestation using an attractive species (Hemigymnus melapterus, Labridae) and an unattractive species (Pomacentrus amboinensis, Pomacentridae). Traps with these fish as a form of bait were deployed to sample blood-sucking gnathiid ectoparasites (Gnathiidae: Isopoda) on reefs from which cleaners (Labroides dimidiatus, Labridae) have been removed for 13 yr. Cleaner fish could not enter traps to access the clients/hosts, but gnathiids could enter the traps to infest hosts; thus, this method sampled the indirect effect of cleaners on gnathiid infestation of fish. Infestation was higher on reefs without cleaners than on those with them. The effect was only detected during the daytime when cleaners are active and only on the attractive species (H. melapterus). Thus, cleaner presence indirectly reduced fish exposure to parasites in a species that is highly susceptible to parasites, but not in one that is rarely infested with parasites. This suggests that cleaner presence indirectly reduces exposure of a common fish species to harmful parasites, which may explain some observed benefits in fishes at this location.

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Acknowledgements

We thank S. P. Blomberg for statistical advice, and field assistants and Lizard Island Research Station staff. This work was funded by the Australian Research Council, Sea World Research and Rescue Foundation, Australia, the US National Science Foundation (OCE-1536794, PC Sikkel, PI), and The University of Queensland.

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Authors and Affiliations

  1. School of Biological Sciences, The University of Queensland, St. Lucia, QLD, 4072, Australia

    A. S. Grutter, M. De Brauwer, K. L. Cheney, T. H. Cribb, E. C. McClure, D. Sun & J. Werminghausen

  2. Department of Biology, University of Neuchâtel, Emile-Argand, 11, 2000, Neuchâtel, Switzerland

    R. Bshary

  3. Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    E. M. P. Madin

  4. Australian Institute of Marine Science, Crawley, WA, 6009, Australia

    M. G. Meekan

  5. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA, 93106, USA

    R. R. Warner

  6. Department of Biological Sciences and Environmental Sciences Program, Arkansas State University, State University, AR, 72467, USA

    P. C. Sikkel

  7. Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom Campus, Potchefstroom, 2520, South Africa

    P. C. Sikkel

  8. Department of Environment and Agriculture, Curtin University, Perth, WA, 6485, Australia

    M. De Brauwer

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  1. A. S. Grutter
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  2. M. De Brauwer
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  6. E. M. P. Madin
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  7. E. C. McClure
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  8. M. G. Meekan
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  9. D. Sun
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  10. R. R. Warner
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  11. J. Werminghausen
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  12. P. C. Sikkel
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Correspondence to A. S. Grutter.

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Grutter, A.S., De Brauwer, M., Bshary, R. et al. Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37, 15–24 (2018). https://doi.org/10.1007/s00338-017-1628-z

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